Eur. J. Entomol. 102: 561–576, 2005
ISSN 1210-5759
POINT OF VIEW
Winter climates and coldhardiness in terrestrial insects
WILLIAM J. TURNOCK and PAUL G. FIELDS*
Cereal Research Centre, Agriculture and Agri-Food Canada, 195 Dafoe Rd, Winnipeg, MB, Canada R3T 2M9
Key words. Winter climates, snow-cover, overwintering, terrestrial insects, winter climatic zones, freeze-tolerance,
freeze-susceptibility, non-freezing mortality, supercooling point, coldhardiness
Abstract. Overwintering insects must avoid injury and death from the freezing of tissues and from metabolic disruptions associated
with exposure to low, non-freezing temperatures. The winter climates of the world are classified in relation to insect overwintering
on the basis of their minimum temperatures and the duration of the winter (when temperatures are below the thermal range for
activity and development). Outside the Tropical Wet zone, the severity of exposure to cold (temperature, snowfall, duration of exposure, predictability, variability) can vary from a few days at 0°C to months below –20°C with extremes as low as –60°C. The
severity of the temperature exposure may be ameliorated by the selection by insects of overwintering sites (exposed, partly-exposed,
protected). The relationships among overwintering habitats, the minimum winter temperature in climatic zones, and the supercooling
points (SCP) of over 350 terrestrial insects from published reports were examined. Variability in the SCP among insects within each
climatic zone and habitat was wide. Among the freeze-susceptible species that overwintered in exposed or partly-protected habitats
the SCP and the cold severity of climate were correlated. This was not the case for insects that overwintered in protected habitats.
The SCP’s of freeze-tolerant insects were generally higher than the freeze-susceptible insects, and the SCP’s were not tightly linked
with the cold severity of climatic zone. Insects, both freeze-susceptible and freeze-tolerant, overwintering in exposed habitats had
lower SCP’s than insects from habitats that offered some protection from ambient temperatures. Thirty-eight species had reports of
SCP’s for different geographical locations. Although there were occasionally differences in the SCP’s, there was no consistent pattern of insects having lower SCP’s when overwintering in colder habitats. The incidence of freeze-tolerance was higher in boreal and
polar climatic zones than in climatic zones with warmer winters. Holometabola insects had a higher incidence of freeze-tolerance
than hemimetabola insects. Suggestions for future research directions are outlined.
INTRODUCTION
The different types and degrees of coldhardiness in
insects are the outcome of adaptations that have enabled
insects to live in environments as severe as those in alpine
and polar regions. Insects have evolved various developmental and behavioural strategies that mitigate the
harmful effects of low temperature (Danks, 1996).
Low temperature damage to insects occurs in two different manners, by injury related to freezing, and by nonfreezing metabolic injury. The formation of ice crystals
may cause physical damage, but metabolic injuries unique
to the frozen state, such as osmotic stress and anoxia, also
affect survival (Storey & Storey, 1987). Non-freezing
metabolic injury is cumulative and can occur at temperatures above the insect's freezing point, but below the
threshold for normal metabolism and development. The
mechanisms through which these low temperatures may
cause injury have not been explained, although several
possibilities have been advanced (Storey & Storey, 1987;
Ramløv, 1999).
Insects use two approaches to avoid freezing-related
injuries. Freeze-susceptible insects have adapted by lowering their supercooling point (SCP) to avoid freezing,
while freeze-tolerant species freeze, but survive freezing
through the action of ice-nucleating agents or the removal
of ice-nucleators from the system. Most freeze-tolerant
species freeze at a relatively high temperature, thereby
avoiding injury associated with the rapid formation of
large ice crystals. However, such frozen insects may die
at a lower temperature (e.g., Vernon et al., 1996). The
cause of such mortality is unknown, but could be related
either to the metabolic injuries unique to the frozen state
(Storey & Storey, 1987) or to the processes involved in
non-freezing injury.
Non-freezing injury is a function of both low temperature and the duration of exposure. The injurious effects
accumulate over time, more quickly at lower temperatures (NedvČd et al., 1998) and can be reversed or
repaired if higher temperatures occur before extensive
damage has occurred (Turnock & Bodnaryk, 1993).
Adaptations to reduce non-freezing injury include lowering the Upper Limit of the Cold Injury Zone (ULCIZ),
and reducing the response to low temperatures and durations of exposure (Turnock et al., 1983, 1998; NedvČd,
1998; Renault et al., 2002).
Coldhardiness research over the past 50 years has
developed an understanding of the impact of freezing on
insect tissues and the mechanisms by which freezing
injury is avoided. The importance of avoiding injurious
low temperatures by behavioural and developmental
mechanisms was recognized, and authors have investigated the microclimates of some overwintering habitats
(Cloudsley-Thompson, 1962; Danks, 1978; Lamb et al.,
1985; Ramløv, 1999; Sinclair, 2001). The SCP has been
used in combination with meteorological data to predict
* Corresponding author; e-mail: [email protected]
561
survival for some species, primarily for those overwintering in exposed habitats (Green, 1962; Sullivan, 1965;
Tenow & Nilssen, 1990; Bale, 1991).
Research on the adaptations used by insects to avoid
non-freezing cold injury has received much less attention
(Renault et al., 2002). A few studies have attempted to
use experimental data on the effect of time and temperature to predict survival (e.g., Lamb et al., 1985; NedvČd et
al., 1998), and some progress has been made in developing techniques for describing the relationship of survival to temperature and duration of exposure (NedvČd,
1998). Adaptations that affect the ability to survive nonfreezing injury appear to be independent of the adaptations to avoid freezing injury (Turnock et al., 1998).
The SCP is no longer deemed an adequate predictor of
overwintering survival for many species (Renault et al.,
2002), but a standard method of predicting survival following exposure to conditions causing non-freezing cold
injury has not yet been accepted. It is clear, however, that
insect species exposed to low temperatures have physiological mechanisms to protect them from both freezing
and non-freezing mortality in their overwintering habitats.
Different climates vary in the intensity of the low temperature stress that they place on insects. Potentially
freezing temperatures may occur for very short periods
(diurnal) or for months. Temperatures potentially causing
non-freezing cold injury also may vary from a few hours
to many months. One would expect that the level of adaptation to protect the insect from each of these low temperature stresses would be related to the conditions experienced by overwintering insects in their overwintering
habitat in the different climatic zones of the world.
As a first step in examining this relationship, we
describe the terrestrial winter climates of the world as
they affect the level of risk from freezing and from cold
injury among overwintering insects in their habitats. We
examined three aspects of insect coldhardiness; SCP,
freeze tolerance and non-freezing injury. The SCP is the
most widely used measure of coldhardiness. Therefore,
we examined the relationship between the SCP and climatic zones by habitat for both freeze-susceptible and
freeze-tolerant species. We also examined the incidence
of freeze-tolerance species among climatic zones and
habitats. Other measures of cold tolerance such as the
duration of survival at low temperatures, the upper limit
of the cold injury zone, the sum of injurious temperatures
are better than SCP for predicting survival at low temperatures. However, few studies have been published, so
our analysis is limited to ways in which resistance to cold
injury varies within and between species. We then pose
some questions about insect coldhardiness that need to be
answered to advance our knowledge of the processes, and
of our ability to predict overwintering survival and the
results of climatic changes on overwintering insects.
WINTER CLIMATES AND INSECT OVERWINTERING
HABITATS
Most classifications of the terrestrial climates of the
world are based on the Köppen system (Köppen, 1931),
562
which considers both summer and winter climates in
establishing five principal groups of world climate. The
Köppen system, as modified by Trewartha & Horn
(1980), provides a basis for looking at world climate from
the standpoint of an overwintering insect (Table 1). Additional information on the colder climates of the world is
found in Grody & Basist (1996), Bailey et al. (1997),
King & Turner (1997), Brown (2000), and Dye (2002). In
this classification of winter climates, we used the major
climatic zones of Trewartha & Horne (1980) – Tropical,
Subtropical, Temperate, Boreal, Polar – but we have
divided their categories of “Dry Climates” and “Highland
Climates” and placed them within the adjacent major
zones. The winter climates of dry areas (steppes and
deserts) are colder, and the diurnal fluctuations are
greater, than in moister areas within the same zone. Climates in highland areas are much more variable than in
lowland and dry climates in the same zone. Diurnal temperature fluctuations are greater than at lower altitudes,
and the topographic variability affects insolation and
wind force, thus increasing variability in the distribution
and persistence of snowcover. We also divided the winter
climates of the Boreal and Polar zones into “Oceanic” and
“Continental” to reflect the effects of open water on the
temperature, cloud cover, and precipitation of these areas.
The elements of climate affecting insects during winter
were selected for the following reasons: (1) the mean air
temperature during the coldest month reflects the
minimum temperature of exposure; (2) the number of
months with mean temperatures below 10°C indicates the
degree of occurrence of temperatures below the threshold
for normal metabolic development of warm-weather
insects, and thus the potential mean upper limit of nonfreezing cold injury; (3) the number of months with mean
temperatures below 0°C indicates the duration of time in
colder climates that an insect might be exposed to
freezing and non-freezing injurious temperatures; (4) the
occurrence and persistence of snowcover greatly affects
the temperature in habitats in soil and on the soil surface.
Snow may also delay the warming of the overwintering
habitat in polar and boreal climates and thus effectively
shorten the summer for species overwintering beneath
thick snowcover.
The zones of winter climate differ in the degree and
duration of stress that they impose on overwintering
insects. Insects exposed to air temperatures must avoid
death from freezing at temperatures as low as –50°C and
survive exposure to temperatures that may cause nonfreezing injury and death for as long as 10 months. However, not all insects overwinter in habitats that are
exposed to air temperature, and both the temperature and
the duration of exposure to low temperatures in less
exposed habitats are modified by topographic and vegetative effects on insolation, insulation, and energy fluxes
(Geiger, 1950; Oke, 1987).
The natural overwintering habitats were classed
according to their degree of exposure to ambient air temperature as: (1) exposed: overwintering on vegetation
(e.g., trees, shrubs) or other structures above the ground
563
3
Highlands
5
6
7
Dry
Cold Continental
Highlands
11
Continental
<–28
ca –15
–18
ca –0
–5 to –18
–4 to –18
0 to –27
ca –4
2–7
12
12
9–10
11
9–11
6–7
5–9
3–7
3–6
2–3
1
1–2
1–2
0
0
0
0
9–10
6–9
6–8
6–8
5–8
4–7
2–7
2–5
0
1–2
0
0
0
0
0
0
0
persistent, <11 mo.
in drifts
sparse, persistent
in drifts
frequent, heavy,
short duration
persists 4–7 mo.
1–2 m deep
occasional,
temporary
occasional,
non-persistant
rare, non-persistant
persists 1–4 mo.,
<1 m deep
persists 1–5 mo.
variable depth
none
rare, transient
rare, transient
occasional,
temporary
none
none
none
rare, transient
Snow
cover
–
–22.5**
–
–19.0a
–19.7a
–32.7*
–21.9a
–17.6a
–
–8.0*
–
–8.1*
–
–
–
–
–37.8
–23.3
–31.0**
–15.6**
–19.2a
–26.6b
–27.8
–19.3a
–16.2a
–16.7
–17.7
–13.4**
–18.3*
–8.3**
–
–9.5
–10.2
–31.5 ± 1.8 (20)
–20.2 ± 1.0 (30)
–20.9 ± 1.2 (47)
–20.0 ± 1.3 (7)
–15.1 ± 1.9 (9)
–13.4 ± 3.5 (2)
–17.0 ± 4.8 (3)
–8.3 ± 4.8 (2)
–
–9.5 ± 0.5 (12)
–10.0 ± 0.7 (16)
–
–
–47.1
–33.6b
–37.8 ± 13.8 (2)
–23.3 ± 2.9 (4)
–39.7 ± 4.7 (11)
–15.6 ± 6.0 (2)
–24.5 ± 1.4 (40)
–34.1c –26.8 ± 0.7 (130)
–39.6
–21.9a
–27.7b
–22.5
–15
–
–24.5*
–
–
–
–8.2*
–
–
–10.5**
–
–7.3
–7.3a
–8.5*
–5.8**
–4.8
–6.4*
–4.6*
–
–
–
–
–
–6.3
–8.7
–4.2
–54.0*
–
–5
–9.1a
–20.2**
–22.5*
–8
–6.6**
–
–
–
–
–
–
–
–
–
–22.9
–
–21
–18.7b
–2.9
–9.2
–
–
–
–
–22.8
–
–
–
–
–8.7 ± 1.3 (7)
5.4, 3.0,
–4.2 ± 0.5 (4)
–23.4 ± 3.9
(13)
–7.7 ± 1.3 (15)
–19.7 ± 7.1 (6)
–10.1 ± 1.0
(41)
–9.9 ± 1.9 (9)
–5.6 ± 0.5 (12)
–6.5 ± 0.2 (3)
–22.8 ± 2.2 (5)
–4.6 (1)
–
–
–
–6.0 ± 0.7 (3)
Freeze-tolerant SCP Mean (°C)
All habitats
PartiallyAll habitats
PartiallyProtected
Exposed
Protected
Exposed Mean ± SEM
protected
Mean ± SEM (N)
protected
(N)
Freeze-susceptible SCP Mean (°C)
Totals
–18.8 ± –20.4 ± –31.5 ±
–6.6 ± –10.0 ± 1.2 –19.0 ± 1.9
0.8 (80)a 0.7 (161)a 0.9 (103)b
0.4 (39)a (52)a
(32)b
Number of observations >2 except * = 1, ** = 2. Standard Error of the Mean (SEM) for individual climates and habitats ranged from 0.2 to 13.0. Different letters following means within the
Temperate zone and totals show significant differences among climatic zones based on Tukey’s Multiple Range Test, P < 0.01. Freeze-susceptible and freeze-tolerant groups were analyzed
separately.
10
9
Oceanic
Polar
Continental
Oceanic
8
4
Warm Continental
Boreal
2
Oceanic
Temperate
5–13
4–13
4–12
1
1
1
3–10
23–27
18–24
ca 23
12–15
1
1
1
1
Cold
Mean air
Months
Months
ranking temperature (°C) below 10°C below 0°C
Tropical
Wet
Wet and dry
Dry
Highlands
Subtropical
Humid
Dry Summer
Dry
Climatic
zone
TABLE 1. Classification of winter climates and the mean SCP of terrestrial insects overwintering in different habitats within these climatic zones.
surface and snowcover; (2) partially-protected: overwintering in vegetation or ground surface litter; or (3) protected: overwintering beneath the soil surface. Insects in
polar and alpine climates tend to be limited in their overwintering habitats to a narrow, biologically-active, zone
between bedrock or permafrost and the top of sparse,
low-growing vegetation.
The temperatures in these habitats vary in their relation
to air temperatures in different climatic zones as well as
varying in response to such variables as snowcover, wind,
precipitation, soil type, and vegetation. Of these, snowcover is the major modifier of the temperature of
partially-protected and protected habitats. Even small
amounts of snow on the foliage of conifers may protect
overwintering insects (e.g., Neodiprion sertifer eggs on
pine branches in Boreal forests; Sullivan, 1965).
In climatic zones where freezing temperatures are associated with temporary invasions of cold air masses (Subtropical, Temperate Oceanic, Temperate Warm Continental, and Temperate Dry), even non-persistent snowfall can
protect insects in partially-protected overwintering habitats. In these areas insects in exposed habitats experience
the minimum air temperatures, while those in protected
habitats are buffered. Partially-protected habitats can be
protected from extremes of low temperature if invasions
of cold air are accompanied by snow.
In climatic zones with persistent, deep snowcover, all
habitats beneath the snow are protected from the fluctuations of air temperatures. With sufficient snowcover,
insects overwintering in the litter, or on soil surfaces can
be considered to occupy protected habitats. Although the
depth and insulation properties of snowcover vary within
the Temperate Cold Continental and Boreal zones, an
insulating blanket of snow can maintain soil temperatures
at levels similar to those in the Temperate Warm Continental zone, where snowcover does not persist.
The climatic zones and overwintering habitats can be
grouped on the basis of their temperatures and duration of
exposure (Table 1).
Tropical Climates
There is no winter, and only in the Highlands do
diurnal temperatures fall below 0°C. Minimum temperatures decrease with altitude, and may be as low as –20°C
at altitudes above 3000 m. Temperatures in the Tropical
Wet and Wet and Dry climates are rarely below 10°C and
do not impose any low temperature stress on insects.
Diurnal frosts in Tropical Dry climates are mild with
short durations, and both air and soil temperatures rise
rapidly during the day. Insects need some protection from
freezing, but the duration of temperatures below 10°C
seems too short to cause non-freezing injury.
Subtropical Climates
Winters are short and mean air temperatures are below
10°C for 1–3 months. Cold air masses bring occasional
brief periods of freezing air temperatures, rarely accompanied by snow. Insects in exposed habitats need some
resistance to freezing, and all habitats have short periods
of temperatures that could cause cold injury. Subtropical
564
Humid and Dry Summer climates do not expose insects to
severe stress from either freezing or non-freezing injury,
regardless of their overwintering habitat. Insects in Subtropical, Humid, and Dry climates are exposed to some
diurnal freezing during occasional short periods of
freezing weather associated with invasions of cold air.
Snow is rare and transient, providing no insulation.
Temperate Climates
There is a definite winter season during which air temperatures are below 10°C and, in all but the Oceanic zone,
below 0°C for 3–8 months. The depth and persistence of
snowcover is a factor modifying the impact of air temperatures in the soil and on the ground surface. Where
snowcover is not persistent, insects overwintering on
vegetation or on the soil surface are exposed to the fluctuating temperatures, similar to air temperatures, that are
associated with invasions of warm and cold air masses.
The variability in the severity of the minimum temperature and the duration of exposure to low temperatures
among the habitats and sub-zones in the Temperate zone
is greater than in other zones. Therefore the level of adaptations to avoid freezing and non-freezing injury also
should be more variable than in other zones.
The Temperate Oceanic and Warm Continental climates do not expose overwintering insects to very low
minimum temperatures, but potentially injurious nonfreezing temperatures may persist for 3–6 months. Insects
overwintering in exposed and partially-protected habitats
may be exposed to temperatures fluctuating above and
below the ULCIZ due to alternating invasions of polar
and subtropical air masses. Such insects may be adapted
to repair injuries in warmer weather following cold
periods (Casagrande & Haynes, 1976; NedvČd et al.,
1998). Snowcover may temporarily protect insects on the
soil surface from low minimum temperatures.
The winters in the Dry climates are colder and drier,
and all the overwintering habitats have lower temperatures than those in the Oceanic and Warm Continental climates. Snowfalls are light and do not persist for long
periods. Winter air temperatures in Temperate Cold Continental climates are well below –10°C, and freezing temperatures persist for 4–7 months. Where snowfall is
heavy and persistent, temperatures on and in the soil are
much warmer than the air temperatures, and generally
remain above –10°C.
Boreal Climates
The winters are long and cold. The short winter days
and limited solar heating reduce diurnal fluctuations.
Polar air masses with low temperatures are dominant.
Snowfall is moderate to heavy and persists (French &
Slaymaker, 1993). Surrounding waters in Boreal Oceanic
zones ameliorate the severity of polar air masses so that
mean air temperatures remain close to 0°C. There is little
variability in daily and seasonal temperatures, and
freezing may occur throughout the year (Klok & Chown,
1997). Snowfalls may be heavy but usually are soon
melted by rains. In contrast, Boreal Continental climates
often have minimum air temperatures below –40°C, but
surface and soil temperatures usually remain above –15°C
because snow is persistent and usually heavy enough to
protect these habitats from air temperature fluctuations.
Polar Climates
The winters are long and days are very short so that
diurnal fluctuations of air temperatures are small. Snowfall is generally light (a very cold desert), and high winds
keep some areas snow free, while forming drifts in other
areas. Permafrost limits overwintering habitats in the soil,
and the areas in which snowdrifts normally form may not
be utilized by overwintering insects because slow melting
of the snow in the spring shortens the already critically
short summer (Danks et al., 1994). Islands in the Arctic
and those close to the Antarctic continent that are surrounded by sea-fast ice in the winter do not differ from
Polar Continental areas during this season (King &
Turner, 1997). Antarctic islands with Polar Oceanic climates have little variability in daily or seasonal temperatures, and freezing temperatures can occur throughout the
year. The tundra climates of the Northern hemisphere
have air temperatures below –50°C, and overwintering
insects need to be well-protected against both freezing
and non-freezing injury.
Highland Climates
These climates are difficult to characterize because the
zonal climate is modified by differences caused by altitudinal variability, degree of exposure to prevailing wind
patterns, sparse vegetation, shallow soils above rock, and
variable snowcover. Diurnal frosts in Tropical Highlands
are mild and of short duration. Insectan habitats warm
rapidly during the day. Some resistance to freezing and
non-freezing injury is needed. In Subtropical Highlands,
diurnal freezing temperatures occur more frequently and
are lower than in the Tropical Highlands, but temperatures rise quickly under strong insolation. Occasional
snows do not persist at altitudes occupied by insects.
Mean monthly temperatures below the activity threshold
occur for 2–3 months, so resistance to both types of
injury are needed by overwintering insects. Temperatures
in the Temperate Highlands are colder than in lower areas
at the same latitude. Snowfall is variable and persists in
some habitats. Freezing temperatures occur for 5–8
months, and overwintering insects need resistance to
freezing and non-freezing injury. Temperate Highlands
that are influenced by air masses from oceans combine
diurnal freeze/thaw cycles with longer cold periods (Ramløv, 1999; Sinclair, 2001; Sinclair et al., 2003). In such
habitats, the ability to survive frequent exposures to
freezing temperatures must be combined with resistance
to, or repair of, cold injury and the rapid reactivation of
metabolic processes as temperatures rise.
WINTER CLIMATES AND INSECT FREEZING
The extensive literature on the SCP of insects was
examined to determine if there is a relationship between
the SCP and winter temperatures. From each report, the
species, strategy (freeze-susceptible or freeze-tolerant),
stage of development, overwintering habitat, location, and
SCP were extracted and the climatic zone of the location
was determined. In most cases the original publications
were examined, but information on some species was
extracted from review articles such as CloudsleyThompson (1970), Lozina-Lozinskii (1974), Merivee
(1978), and Sømme (1982). References for individual
species are not cited, except for species that are discussed.
Sources of error in these records include the use of different techniques in measuring the SCP and the lack of
precise information on overwintering habitats. This data
base is limited to terrestrial insects in their natural habitats, and it is available from the authors. The considerable
literature on insects in glasshouses and grain bulks, and
on Collembola and Arachnida was not considered.
The information on freezing-susceptible (338 records
for 268 species) and freezing-tolerant (120 records for 94
species) insects was analysed separately. Preliminary
analyses of the SCPs of Hemimetabola and Holometabola
showed a similar relationship to climate and habitat, so
they were combined in the analyses. The distribution of
records does not cover all the climatic zones and habitats,
and several have only a few records.
Variations Among Species by Climatic Zones
The SCP of overwintering insects was related to the
severity of the winter temperatures, although variability
was high both within and among climatic zones and habitats (Fig. 1). Correlation analyses were conducted for
both freeze-susceptible and freeze-tolerant species
between the ranking of the severity of the winter temperature (Table 1) and the SCPs in each climatic zone and
habitat with sufficient records (Fig. 1). The correlation
was significant among freeze-susceptible insects in
exposed and partially-protected habitats, but not in protected habitats. For freeze-tolerant insects there was no
correlation between SCP and cold severity in exposed and
partially-protected habits. There was a correlation in protected habitats, but the range of SCP values was narrow.
The mean SCP of both freeze-susceptible and freezetolerant insects overwintering in exposed habitats was
significantly lower than in the other habitats (Table 1).
For freeze-susceptible insects, this difference among
habitats did not occur in the Tropical zone or in the
warmer climates (Humid, Dry Summer) of the Subtropical zone. For freeze-tolerant species, a significant
difference between the exposed and the other habitats
occurred only in two of the climates with the lowest
winter temperatures, the Temperate Highland and Boreal
Continental climates.
In Tropical Climates, the mean SCP of freezesusceptible insects ranged from –8.2 to –10.2°C (Table
1). The SCPs for individual species were all above
–13.0°C, except for two species from the Tropical Highlands: Cossonus frigidus Schiødte (–17.5°C) and Brachycaudus helichrysi (Kaltenbach) (–25.1°C) (Sømme &
Zachariassen, 1981). Both of these species are normally
exposed to lower night temperatures than the other 14
species reported by these authors from high altitudes on
Mount Kenya, C. frigidus because it inhabits dry rather
than wet plant material, and B. helichrysi because it was
565
Fig. 1. The variation in SCP of freeze-susceptible and freeze-tolerant insects, grouped by habitat (Table 1) and ranked by cold
severity. A Spearman Rank Order Correlation was conducted for each data set.
collected from the highest altitude sampled, 4985 m,
where night temperatures are likely below –20°C. The
SCPs of three species of freeze-tolerant insects from
exposed Highland habitats ranged from –4.8 to –7.3°C.
In Subtropical Climates, the SCPs of freeze-susceptible
species was high (–8.1, –8.0°C) in protected habitats,
lower (–13.0 to –18.0°C) in partially-protected habitats,
and lowest (below –20.0°C) in exposed habitats of the
Dry and Highlands zones (Table 1). The lowest SCP in
the Humid and Dry Summer zones was for Helicoverpa
(Heliothis) zea (Boddie), the cosmopolitan pest of maize
(Roberts et al., 1972). Most of the freeze-tolerant species
had high SCPs (–4.6 to –6.6°C), but three species from
the subtropical dry zones had SCPs from –26.0 to
–29.0°C, Eurytoma obtusiventris Gahan, Eurytoma
gigantea Walsh, and Mordellistena unicolor Leconte.
These species inhabit goldenrod galls and have a wide
distribution in more northerly climates (Baust et al., 1979;
Duman & Montgomery, 1991).
In Temperate Climates, freeze-susceptible insects show
increasingly lower SCPs from protected, through
partially-protected, to exposed habitats (Table 1). The
mean SCP in exposed habitats was significantly lower
than in the other habitats in the Oceanic, Cold
Continental, and Highlands zones. Only in the Cold Continental zone was the mean SCP in the partially-protected
habitat significantly lower than in the protected habitat.
The SCPs of freeze-tolerant insects in all Temperate
zones were mainly above –15°C (86%, N = 82). The 10
species with SCPs below –15°C included the three species from goldenrod galls (Baust et al., 1979) that are also
566
found in the Subtropical Dry zone (see above); Ostrinia
nubilalis (Hubn.) in the Temperate Oceanic, Warm Continental, and Cold Continental zones (Barnes & Hodson,
1956; Hanec & Beck, 1960; Grubor-Lajsic et al., 1991),
Bracon cephi (Gahan) a parasitoid of the wheat stem sawfly, Cephus cinctus Nort. (Salt, 1959), and Macdunnoughis confusa Stph. (Merivee, 1978). All of these have
widespread distributions and overwinter in habitats where
snowcover is minimal, either in open grasslands or in
crop residues on the soil surface. The mean SCP of species in exposed habitats of the Cold Continental zone was
significantly lower than in the other habitats.
In Boreal Climates, the mean SCP of freeze-susceptible
species was higher in the Oceanic than Continental zones
(Table 1). In the Continental zone, the mean SCP
decreased from –22.7°C in protected habitats, to –31.0°C
in partially-protected habitats, to –47.1°C in exposed
habitats. The first two habitat types are protected from
low air temperatures by a cover of snow that is generally
deep and persistent. Insects in these habitats have only
slightly lower SCPs than insects overwintering in similar
habitats in the Temperate Cold Continental zone. Among
nine species from partially-protected and exposed
habitats, only one, Rheumaptera hastata (L.), had a SCP
(ca –24.0°C; Werner, 1978) higher than –31.0°C, and the
others had SCPs from –31.0 to – 58.0°C. The 10 freezetolerant species from exposed habitats (SCPs –6.2 to
–36.0°C) were all collected under dead or loose bark in
the interior of Alaska, USA, above the deep and persistent snowcover (Werner, 1978). In protected habitats in
the same location, Pterostichus brevicornis Kirby had a
SCP of –11°C. In partially-protected habitats in the
Rocky Mountains, the SCP of Pytho planus (deplanatus)
Olivier was –54.0°C (Ring, 1982).
In Polar Continental Climates, where air temperatures
are very low, snowfall light, and winds strong, most
insects overwinter in partially-protected habitats. The
SCPs of two freeze-susceptible species from Arctic
Canada were –24.0 and –51.6°C (Ring & Tesar, 1980;
Ring, 1982), while those of seven freeze-tolerant species
ranged from –6.0 to –17.3°C. Polar Oceanic climates are
less severe. Among species from Antarctic islands, the
SCPs of freeze-tolerant species were –3.0 and –5.4°C (N
= 2), and of freeze-susceptible species from –18.9 to
–28.7°C (N = 3).
Variation Within Species Among and Within Climatic
Zones
The mean SCP for a species has been reported for more
than one population within a climatic zone or from populations from more than one climatic zone for 25 species of
freeze-susceptible (Table 2) and 13 species of freezetolerant insects (Table 3). The mean SCP reported from
these studies may be influenced by the source of the
material, small sample size, and differences in technique
in determining the freezing point. The degree to which
such influences have affected the mean SCP cannot be
determined from the published information. We accepted
that SCPs differing by 4°C or more were evidence of a
real difference among species or populations.
Among the 24 freeze-susceptible species for which
records from more than one location within a climatic
zone were available (Table 2), the difference was less
than 4°C for 9 species in 12 climatic zones. Their mean
within-zone difference in SCP records was 1.4°C.
Although there were occasionally differences in the
SCP’s, there was no consistent pattern of insects having
lower SCP’s overwintering in colder habitats.
The difference of 4.0°C between populations of Rhopobota naevana (Hübner) in western (warmer) and eastern
(colder) parts of southern Norway (Temperate Cold Continental zone) is consistent with differences in winter temperatures (Sømme, 1965). There are large differences
among populations of Neodiprion sertifer Geoffr. within
the Temperate Cold Continental climate of Estonia and
Latvia, –34.1°C (Sullivan, 1965); –39.1 to –40.6°C
(Kopvillem & Kuusik, 1971; Merivee, 1978) but not
among populations in Japan and Canada (–30.8° and
–32.1°C) or between those and populations in the Temperate Highlands of Europe (–30.1 to –32.0°C) (Sullivan,
1965). Similar differences occur between populations of
D. radicum from Estonia (–25.2°C; Merivee, 1978) and
Leningrad (ca –21°C; KošĢál, 1993) but Turnock et al.
(1998) found no relationship between the SCP and the
mean January air temperature for populations of this species from different locations and climatic zones. Differences within climatic zones in the SCPs of these two
species are probably related to the experimental techniques of different researchers, but the difference of 10°C
between reports for Dendroides canadensis Latreille, by
the same researchers (Duman, 1980; Olsen & Duman,
1997) cannot be explained.
Among 16 freeze-susceptible species that were examined from more than one climatic zone, 5 have SCPs that
differ among zones (Table 2). In Canada, the fall cankerworm, Alsophila pometaria (Harris), has a lower SCP in
the Temperate Dry climate of Alberta (–44.6°C; Sømme,
1964), than in the Temperate Cold Continental climate of
Nova Scotia (–37.2°C; MacPhee, 1964). The SCP of Neodiprion pratti banksianae Rohwer in Canada is higher in
the Temperate Cold Continental zone (–34.0°C) than that
in the colder Boreal Continental zone (–39.1°C)
(Sullivan, 1965). The European elm bark beetle, Scolytus
multistriatus (Marsham), freezes at a higher temperature
in the Temperate Cold Continental climate of Michigan,
USA, (–24.1°C; Truchan & Butcher, 1970) than in the
colder Boreal Continental zone of mid-Asia (–53.0°C;
Lozina-Lozinskii, 1974). Differences in the SCP that are
correlated with differences in the mean January temperature are also recorded for Pyrrhocoris apterus (L.) in Bulgaria and the Czech Republic (Kalushkov & NedvČd,
2000; Hodková & Hodek, 1994). Exochomus quadripustulatus (L.) is anomalous, with an SCP of –13.5°C in the
Temperate Cold Continental zone at Leningrad (Pantyukhov, 1971) and –24.0°C from the Temperate Warm Continental zone in southern Bohemia (NedvČd, 1993).
The SCP of most freeze-susceptible species does not
vary greatly within their range of occurrence, but four
species show a variation in their SCP that is correlated
with temperature differences both within and among climatic zones (Table 2). Three of the four species overwinter on the twigs, branches, or bark of trees in the
colder Temperate zones, while the fourth overwinters in
litter in the Subtropical Dry and Temperate Warm Continental zones.
Variation within or among climatic zones in the SCP of
freeze-tolerant species was generally small (Table 3). The
distribution of insect species inhabiting the galls of goldenrod in North America includes several climatic zones.
The SCPs of populations of goldenrod gall fly, Eurosta
solidaginis in the Suptropical Dry climate of Texas varied
from –10.0 to –18.2°C (Baust et al., 1979), but populations in the Temperate Cold Continental and Temperate
Dry zones only varied from –9.6 to –13.7°C (Sømme,
1964, 1978; Baust et al., 1979; Baust & Lee, 1981;
Rickards et al., 1987). The SCP of another species in
goldenrod galls, E. gigantea, varied from 23.0°C (Temperate Cold Continental climate, cold with heavy snow
fall), –27.0°C (Subtropical Dry climate, rarely cold and
little snow), to –49°C (Temperate Dry climate, cold, little
snow, Brown, 2000). The SCPs of another widespread
species, the European corn borer, O. nubilalis, differed
among the Temperate Warm Continental climate of
Yugoslavia (–22.5°C, Grubor-Lajsic et al., 1991) and the
Temperate Cold Continental climate of St. Petersburg,
Russia (–25.0°C, Lozina-Lozinskii, 1974), Minnesota,
USA (–22.0°C) and Wisconsin USA (–18.6°C, Barnes &
Hodson, 1956; Hanec & Beck, 1960).
567
TABLE 2. Comparison of the SCP of freeze-susceptible insects within and among winter climates.
Species
Hippodamia convergens
Dendroides canadensis
Rhopobota
(Acrolita) naevana
Temperate Warm Continental
Location
CA USA
Leeds UK
Wales UK
IN USA
Temperate Cold Continental
Norway
–26.0, –30.0
Sømme, 1965
Amphipoea fucasa
Temperate Cold Continental
Japan
Estonia
–36.2
–35.7
Temperate Cold Continental
Japan
–24.0, –24.9
Temperate Highlands
Norway
Temperate Highlands
Norway
Tropical Wet
Subtropical Humid
Temperate Warm Continental
Temperate Warm Continental
Tropical Wet
Subtropical Humid
Temperate Warm Continental
Temperate Oceanic
Temperate Oceanic
Temperate Cold Continental
Temperate Oceanic
Temperate Cold Continental
Temperate Cold Continental
Temperate Cold Continental
Temperate Cold Continental
Temperate Dry
Temperate Dry
Temperate Dry
Temperate Dry
Hainan China
Anhui China
Hebei China
Liaoning China
Ishigaki Japan
South Japan
Akita Japan
Norway
Leeds UK
Estonia
Australia
NS Canada
Belgorod Russia
Poltava Ukraine
St. Petersburg Russia
Tadzikistan
Yessentuki Russia
Samarkand Uzbekistan
Karaganda Kazakstan
BC Canada
UK
Estonia
St. Petersburg, Russia
QC Canada
MB Canada
CN USA
MS USA
QC Canada
Estonia
Latvia
ON Canada
Japan
Austria
Germany
Switzerland
Czech Rep.
Russia
UK
Norway
Bulgaria
Czech Rep
Caucasus Russia
Tambov Russia
AR USA
IL USA
Mexico
OH USA
MN USA
NY USA
NS Canada
AB Canada
USA
mid-Asia
ON Canada
ON Canada
–33.8, –34.3
–17.0, –19.0,
–27.9
–23.7
–25.5
–25.2
–23.6
–38.0
–27.0, –27.3
–27.4
–25.8, –25.0
–23.9
–26.4, –25.5
–23.5
–27.2
–24.9
–24.6
–24.2
–25.1
–24.0
–24.0
–24.0
–24.8
–24.0
–25.2
–24.8
–24.1
ca. –21.0
–30.2
–27.7–0
–30.2, 30.5
–40.6
–39.1, –34.5
–32.1
–30.8
–32.0
–31.3
–31.1
–24.0
–13.5
–22.6
–21.6
–9.5
–16.8
–21.8
–21.2
–22.2
–22.3
–21.1
–22.3
–17.4
–18.4
–37.2
–44.6
–24.1
–53.0
–34.0
–39.1
Tsutsui et al., 1987
Merivee, 1978
Shimada et al., 1984;
Sakagami et al., 1985
Gehrken 1984; Satvedt, 1975
Zachariassen & Hammel, 1976;
Zachariassen, 1980; Gehrken, 1992
Myzus persicae
Leguminivora
glycinivorella
Ips acuminatus
Rhagium inquisitor
Locusta migratoria
Psacothea hilaris
Pieris brassicae
Laspeyresia pomonella
Climate
Subtropical Highlands
Temperate Oceanic
Delia radicum
Temperate Oceanic
Temperate Cold Continental
Lymantria dispar
Temperate Warm Continental
Temperate Cold Continental
Neodiprion sertifer
Exochomus
quadripustulatus
Craspedoleta
nebulosa
Pyrrhocoris
apterus
Euproctis
chrysorrhea
Heliothis zea
Dalbulus maidis
Coleomegilla
maculata
Alsophila
pometaria
Scolytus
multistriatus
Neodiprion
p. banksianae
568
Temperate Cold Continental
Temperate Cold Continental
Temperate Cold Continental
Temperate Cold Continental
Temperate Highlands
Temperate Highlands
Temperate Highlands
Temperate Warm Continental
Temperate Cold Continental
Temperate Oceanic
Temperate Highlands
Subtropical Dry Summer
Temperate Warm Continental
Temperate Cold Continental
Temperate Dry
Subtropical Humid
Temperate Cold Continental
Subtropical Highlands
Temperate Cold Continental
Temperate Cold Continental
Temperate Cold Continental
Temperate Dry
Temperate Cold Continental
Boreal Continental
Temperate Cold Continental
Boreal Continental
SCP (°C)
–16.0, –18.2
–27.5
–26.6
–12.0, –22.0
Reference
Lee, 1980; Bennet & Lee, 1989
O’Doherty & Bale, 1985;
Bale et al., 1988
Duman, 1980; Olsen & Duman, 1997
Jing & Kang, 2003
Shintani & Ishikawa, 1999
Sømme, 1967; Pullin et al., 1991;
Pullin & Bale, 1989; Hansen & Merivee,
1971; Merivee, 1978
Shel’deshova, 1967
MacPhee, 1964
Shel’deshova, 1967
Turnock et al., 1998
Turnock et al., 1985
Merivee, 1978
KošĢál, 1993
Turnock et al., 1990
Denlinger et al., 1992
Sullivan & Wallace, 1972
Madrid & Stewart, 1981
Kopvillem & Kuusik, 1971;
Merivee 1978;
Sullivan, 1965
NedvČd, 1993
Pantyukov, 1971
Bird & Hodkinson, 1999
Kalushkov & NedvČd, 2000
Hodkova & Hodek, 1994
Pantyukov, 1964
Roberts et al., 1972
Larsen et al., 1993
Johnson & Lee, 1990
Baust & Morrissey, 1975
MacPhee, 1964
Sømme, 1964
Truchan & Butcher, 1970
Lozina-Lozinskii, 1974
Sullivan, 1965
TABLE 3. Comparison of the SCP of species of freeze-tolerant insects with more than two records within or among different
winter climates.
Species
Climate
Location
SCP (°C)
Reference
Phyllodecta laticollis
Temperate Highlands
Norway
–7.0
–5.0
Van der Laak, 1982
Zachariassen, 1980
Melasoma collaris
Temperate Highlands
Norway
–5.0
–7.3
Zachariassen, 1980
Gehrken & Southon, 1997
Pytho depressus
Temperate Highlands
Norway
–7.0, –5.0
Zachariassen 1977, 1980
Pterostichus brevicornis
Boreal Continental
AK USA
–10.0, –11.0
Miller, 1969, 1982
Belgica antarctica
Polar Continental
Galindez I.
Palmer Sta
–6.2
–5.7
Block, 1982
Baust & Edwards, 1979
Ostrinia nubilalis
Temperate Warm Continental
Temperate Cold Continental
Yugoslavia
St. Petersburg
Russia
MN USA
WI USA
–22.5
–25.0
–22.0
–18.6
Grubor-Lajsic et al., 1991
Lozina-Lozinskii, 1974
Barnes & Hodson, 1956
Hanec & Beck, 1960
Pytho planus (americanus)
Temperate Highlands
Polar Continental
BC Canada
NWT Canada
–6.6
–6.0
Ring, 1982
Ring & Tesar, 1980
Pytho planus (deplanatus)
Temperate Highlands
BC Canada
–54
Ring, 1982
Eurosta solidaginis
Subtropical Dry
Temperate Dry
Temp. Cold Cont.
TX, USA
AB Canada
ON Canada
MN USA
NY USA
–18.2, –10.0
–10.1 ,–9.6
–10.5
–10.2
–13.7
Baust et al., 1979
Sømme, 1964, 1978
Rickards et al., 1987
Baust & Lee, 1981
Baust et al., 1979
Eurytoma gigantea
Subtropical Dry
Temp. Cold Cont.
Temperate Dry
TX USA
NY USA
AB Canada
–27.0
–23.0
–49.0
Baust et al., 1979
Sømme, 1964
Eurytoma obtusiventris
Subtropical Dry
Temp. Cold Cont.
TX, USA
NY, USA
–29.0
–29.0
Baust et al., 1979
Mordellistena unicolor
Subtropical Dry
Temp. Cold Cont.
TX, USA
NY, USA
–26.0
–26.0
Duman & Montgomery, 1991
Baust et al., 1979
Temperate Highlands
Temp. Cold Cont.
Temp. Cold Cont.
Norway
Japan
Estonia
–5.5
–8.3
–5.7
Zachariassen, 1980
Ohyama & Asahina, 1972
Merivee, 1978
Phosphuga atrata
PROPORTIONS OF SPECIES ADOPTING
FREEZE-TOLERANCE VS -SUSCEPTIBILITY
The incidence of freeze-tolerance among species overwintering in exposed habitats tended to be lower than
among those in partially-protected or protected habitats
(Table 4). However, the differences were statistically significant only among species in Temperate Zone Cold
Continental and Dry climates. With the data pooled for all
habitats within climatic zones, the incidence of freezetolerance was significantly higher in the Boreal and Polar
zones than in the Tropical and Temperate zones.
Differences between the incidence of freeze-tolerance
among insects in the southern and northern hemispheres
led Sinclair et al. (2003) to conclude that this strategy
would be selected for under conditions with “the certainty
of severe, sub-zero cold” and “the unpredictability of
non-frigid freeze-thaw events”. The high incidence of
freeze-tolerance in Polar and Boreal climates supports the
first case, but the incidence is generally low among overwintering insects in exposed habitats in the Temperate
zone (Table 4). Within the Temperate zone, partlyexposed and exposed overwintering habitats in the Oceanic and Warm Continental have unpredictably variable
winters in which “non-frigid, freeze-thaw events” are
likely, and would be expected to favour the freezetolerant strategy. Although the incidence of freezetolerance is highest in the exposed habitats of Warm
Continental climates, it is also high in protected habitats
in these climates (Table 4). The overwintering microhabitat may also play a role. For example, among beetle
species inhabiting rotten stumps in the Temperate Oceanic zone of France (Vernon et al., 1996), the incidence
of freeze-tolerance is high although they are protected
from rapid temperature changes. Contact with water may
prevent supercooling and necessitate the ability to tolerate
freezing (Fields & McNeil, 1986).
Freeze-tolerance has not been recorded among the eggs
of overwintering terrestrial Hemimetabola or Holometabola (Table 5). In the other developmental stages, the
incidence of freeze-tolerance was significantly (P < 0.02)
higher among the Holometabola (27%) than among the
Hemimetabola (12%). Among Holometabola the incidence of freeze-tolerance was significantly lower for
pupae than for larvae or adults, but there were no consistent differences in the incidence among species overwintering in different habitats. In the Hemimetabola, there
were no significant differences in the incidence of freeze-
569
TABLE 4. The percentage of freeze-tolerant species among overwintering terrestrial insects by overwintering site and climatic
zone. (Number of records in parentheses) 1.
Freeze tolerance (%)
Climatic zone
Tropical
Subtropical
Temperate (all)
Oceanic
Warm Continental
Cold Continental
Dry
Boreal
Polar
All zones
Protected habitat
Partially-protected habitat
Exposed habitat
All habitats
100(3)
50(4)
30(92)a
47(19)
33(6)
21(44)b
35(23)b
50(4)
—
34(103)a
0(29)
25(8)
27(121)a
15(20)
7(13)
36(66)b
23(22)a
20(5)
71(17)
27(180)a
100(1)
31(13)
18(79)a
0(10)
50(10)
13(38)a
19(21)a
59(17)
—
25(110)a
9(33)z
32(25)zyx
26(292)x
24(49)
28(29)
26(148)
26(66)
50(26)y
71(17)y
1
Subdivided contingency tables were used to test if habitats (rows) or if climate zones (columns) affect the proportion that was
freeze-tolerant. Fisher exact test and Bonferroni inequality were used to adjust tests and P values when required, P < 0.05, no test if
there were insufficient numbers.
tolerance among the developmental stages or among habitats (Table 5).
WINTER CLIMATES AND INSECT COLD INJURY
The ability to survive non-freezing cold injury has long
been recognized a factor in insect coldhardiness (see
reviews by Danks, 1978; Bale, 1987; Lee, 1989; Fields,
1992; Sømme, 1999). Despite this, information on the
manner in which insects have adapted to the challenges of
extended exposures to low temperatures above the SCP is
limited. Recent reviews persist in maintaining that the
two main strategies for insect survival in cold are freezetolerance and freeze-susceptibility (Sinclair, 1999;
Sømme, 1999; Renault et al., 2002; Sinclair et al., 2003).
TABLE 5. The percentage of freeze-tolerant species among terrestrial insects by overwintering site among the developmental
stages of Holometabola and Hemimetabola 1.
Freeze tolerance (%)
Stage
Holometabola
Eggs
Larvae
Pupae
Adults
All Stages
Hemimetabola
Eggs
Nymphs
Adults
All Stages
1
Protected Partially protected Exposed
All
habitat
habitat
habitat habitats
0(1)
20(30)a
0(18)a
52(46)b
24(95)a
0(11)
53(64)b
8(26)b
21(73)a
29(174)a
0(14)
0(26)z
26(29)a 37(123)y
50(4)b 8(48)z
45(22)b 30(141)y
25(69)a
0(1)
0(3)
100(1)
20(5)a
0(1)
100(1)
13(15)
18(17)a
0(8)
0(10)
17(12)
7(30)a
0(10)z
7(14)z
18(28)z
Subdivided contingency tables were used to test if habitats
(rows) or if stage (columns) affect the proportion that was
freeze-tolerant. Holometabola and Hemimetabola tested separately. Fisher exact test and Bonferroni inequality were used to
adjust tests and P values when required, P < 0.02, no test if there
were insufficient numbers.
570
It would be more profitable for research to consider that
the two principal physiological adaptations to cold are the
avoidance of freezing injury and the avoidance of nonfreezing cold injury. Our knowledge of the effects of low
temperatures on the physiological processes that are
involved in cold injury and the adaptations that have been
used to avoid this injury is rudimentary. Potential causes
of death at low, non-freezing temperatures are reviewed
by Ramløv (2000) and Renault et al. (2002).
Consensus on the parameters that need to be measured
to characterize the level of cold injury resistance in
insects will not be reached until much more data has been
accumulated, but we believe that the following concepts
are worth pursuing.
Upper Limit of the Cold Injury Zone (ULCIZ)
The ULCIZ, the lowest temperature at which no significant mortality occurred during an ecologically relevant
duration of exposure, is an important characteristic. This
concept was developed in studies of freeze-susceptible
insects overwintering in the soil of Temperate Oceanic
and Temperate Cold Continental climates (Turnock et al.,
1983, 1985, 1998; Turnock & Bilodeau, 1992; Turnock,
1993; Turnock & Carl, 1995). NedvČd (1998) presented
calculations of the ULCIZ for seven species, showing that
the value was below 10°C for a tropical species,
Nauphoeta cinerea Olivier, 1.3°C for a Collembolan
overwintering in the surface litter in a Temperate Oceanic
climate, and –6.6 to –15.6°C among three species overwintering in the soil in a Temperate Cold Continental climate. Among these three species, the ULCIZ (–5° C to
–15°C) varied parallel to the SCP (–20.3 to –26.4°C)
(Turnock, 1993; NedvČd, 1998). These species may differ
in the soil depth at which they overwinter and therefore
are exposed to different winter temperatures. The change
in the ULCIZ of Eurithia consobrina (Meigen) from
–7.5°C among overwintering puparia that were the
progeny of adults from Germany (Temperate Oceanic climate) to –17.5°C for their progeny reared for 5–10 generations with diapause-inducing larval rearing
temperatures and cold exposures of 140 days, shows that
this parameter can be altered by selection (Turnock &
Carl, 1995).
Predicting Survival
The rate at which survival decreases with increased
stress from lower temperatures and longer exposures,
involves the interaction of two variables, and is more difficult to characterize. This relationship has been described
by regression analysis of duration of exposure for several
temperatures (e.g. Merivee, 1978), and a regression equation that combined temperatures and exposures within the
cold injury zone was developed to predict non-freezing
survival (Turnock et al., 1983; Lamb et al., 1985; Turnock et al., 1990; Turnock & Bilodeau, 1992; Turnock,
1993; Turnock & Carl, 1995; Turnock et al., 1998). The
calculation of negative degree-days (DD) below 0°C
assumes that a particular DD accumulation has the same
impact on survival, regardless of the combination of temperature and time that is used (Bale, 1996). The inclusion
of temperatures above the ULCIZ, where no cold injury
occurs, is an obvious flaw in this approach. NedvČd
(1998) reviewed methods of describing this relationship
and proposed the use of the product of time and temperature exposure within the cold injury zone, the sum of
injurious temperatures (SIT), in day-degrees (DD), or
Kelvin-days (KD) (NedvČd, 1998). This approach avoids
the problem noted by Bale (1996), and has merit as a
single parameter to characterize the response of a species
to non-freezing stress (temperature and duration of exposure) within the cold injury zone. NedvČd (2000b) calculated the time needed to cause 50% mortality (LT50) to
illustrate the response to cold injury of Stenotarsus
rotundus Arrow. However, information on the ULCIZ
and SIT is only available for very few species. Much
more data are needed to test the usefulness of these
parameters in helping us to understand the adaptations of
species to avoid cold injury and their relationship to adaptations to avoid freezing injury.
The concept of ULCIZ and SIT may apply to freezetolerant species. Some species do not survive exposure to
temperatures several degrees below their SCP (Fields &
McNeil, 1986, 1988; Vernon et al., 1996; Sømme, 1999).
It seems likely that this mortality is caused by nonfreezing cold injury, but definitive experiments on
time/temperature relationships and the mechanism
causing injury have not been reported.
The concept of ULCIZ and SIT would be of little value
for insects which die only if frozen, i.e no mortality
occurs regardless of the temperature or duration of exposure at temperatures above the SCP (Bale, 1993; NedvČd,
2000a). However, the research on which this class is
based (e.g. Rickards et al., 1987; Tenow & Nilssen, 1990)
does not include a range of time/temperature experiments,
and therefore does not eliminate the possibility that death
from cold injury occurs at temperatures above the SCP.
Such species could provide evidence about changes in the
ULCIZ and SIT that have occurred in insects adapted to
extreme temperatures, if experiments were conducted
with a range of ecologically-relevant temperatures and
exposures.
Other Parameters
Estimates of the Lethal Time to 50% mortality (Ltime
50) and of the Lethal Temperature for 50% mortality
(Ltemp 50) have been used to describe the level of coldhardiness to non-freezing cold injury. The common
design in such studies has been to determine the decrease
in survival among subsamples placed at a constant temperature for different exposure periods (Pullin et al.,
1991) or among subsamples placed at a fixed period of
time at a series of temperatures (van der Woude & Verhoef, 1986). These parameters are not based on a range of
both temperatures and durations of exposure, so they are
not adequate to describe mortality caused by non-freezing
cold injury. However, they may be useful for specific
comparisons.
Repair of Cold Injury
Cold injury may be repaired if suitable temperatures
occur and this adaptation feature appears to be particularly important in species that overwinter in habitats with
variable winter temperatures, e.g. ground-surface litter in
Temperate Warm Continental, Oceanic, and Highland climates (Casagrande & Haynes, 1976; NedvČd et al., 1998;
Sinclair, 2001). This characteristic was also identified in a
species overwintering in the soil, where no such temperature reversals occur (Turnock & Bodnaryk, 1991), but
there is no information on how widely it occurs in other
species. The common experimental design for investigating acclimation ignores the possibility of repairing
cold injury. Experiments where insects exposed to a low
temperature followed by a cool temperature are compared
to those exposed to cool followed by cold temperatures
with survival checked at a warm temperature (e.g.
–20°/5°/25°C, compared to 5°/–20°/25°C; Denlinger et
al., 1992) are not adequate to determine if acclimation
does occur, because increased coldhardiness in the second
group could be the result of repair of cold injury at the
warm temperature. Samples exposed to a low temperature
should be kept for the duration of a normal winter at a
temperature above the ULCIZ, but below the temperature
at which cold injury can be repaired. For Mamestra configurata (Walker) this zone lies between –5°C (ULCIZ)
and ca. 10°C (Turnock & Bodnaryk, 1991, 1993). Temperatures within this zone neither cause cold injury nor
allow the repair of the injury occurring at lower temperatures.
The zone between the minimum temperature at which
normal activities and development occur and the ULCIZ
needs more attention in coldhardiness research. In seasonal climates, most insect species are in diapause or quiescence to minimize the physiological stresses and to
allow the completion of diapause development (Tauber et
al., 1986). Within this zone, temperature does not affect
survival, provided the duration of exposure does not
exceed the normal winter period. The development of
rearing techniques for species living in seasonally cold
climates usually identifies optimum overwintering tem571
peratures, those at which diapause is broken and mortality
is minimal. Such temperatures, maintained for a period
approximating natural winter length, can be used as the
holding temperature in experiments to determine survival
in cold injury studies, as well as giving a basis for experiments to determine the limits of this zone. We propose
that it be named the “maintenance zone”.
DISCUSSION
The results of coldhardiness research should describe
the mechanisms that insects have developed to protect
themselves from low temperature, allow the prediction of
overwintering survival in a particular habitat, and estimate the probability of a species surviving in locations
outside its range. The question as to how well insects are
adapted to their overwintering niches can be only partially answered from the available data. The system of
classification of winter climates and habitats can provide
a useful framework in examining the relationship between
the conditions in the overwintering habitats and the level
of coldhardiness.
The SCP is the best documented parameter for
describing levels of coldhardiness. Among freezesusceptible species in partially-protected and exposed
habitats the SCP decreased significantly with increased
severity of the overwintering habitat. In addition, the
highest SCP decreased with increasing severity of the
overwintering habitat, indicating that a minimum level of
protection against freezing was needed to survive in each
habitat. No such trend occurred among species in protected habitats, suggesting that freezing is not the major
threat to their overwintering survival. The range of values
was high, at least 20°C, regardless of the climatic zone or
habitat. Some of the variability is undoubtably due to the
division of overwintering habitats into only three broad
categories. In other cases, mobile species inhabiting more
than one climatic zone may retain the SCP necessary to
survive in the coldest part of their range. The SCP may
also reflect an adaptation to stresses other than low temperature (metabolic stability during periods of diapause or
quiescence, protection against desiccation) that lower the
SCP. The compounds giving such protection may also be
cryoprotectants, giving a SCP below that needed to avoid
freezing. This basic SCP, when lower than minimum temperatures in an overwintering habitat, precludes the need
for further adaptation in the SCP, and can be considered
as a pre-adaptation for surviving low temperatures. The
mean SCP is a useful parameter for describing the ability
of a species to survive freezing, but its value as a predictor of overwintering survival, or in estimating the
probability of a species surviving under new conditions in
their overwintering habitat is limited. Changes in the
probability of freezing could occur either through an
extension in the geographical range or because of climatic
changes. Useful predictions might be made for species
overwintering in exposed and some partially-protected
habitats, but not for those in protected habitats.
There is less data for freeze-tolerant species, and the
SCP was not significantly related to the severity of the
572
climatic zone and habitat. The range of SCP values
increased with severity and from protected to exposed
habitats. Unlike freeze-susceptible species, some species
found in very cold overwintering habitats have a SCP
about the same as for species found in the warmest climates and habitats. A few species have very low SCPs,
seeming to combine the advantages of cryoprotectants to
avoid freezing with the use of nucleators to avoid the consequences of freezing. Freeze-tolerance, as a method of
avoiding freezing injury, may occur more frequently in
climatic zones and habitats with fluctuating winter temperatures and in those with very low temperatures.
Non-freezing cold injury has been rather poorly
studied. The mechanisms for protecting insects from nonfreezing injury are different from those protecting from
freezing, i.e., some species adequately protected from
freezing in their overwintering habitat are susceptible to
non-freezing injury and death. The converse may also
occur, insects that appear not to be affected by nonfreezing injury die only when temperatures in their overwintering habitat are below the SCP. Non-freezing injury
has been clearly demonstrated in freeze-susceptible species, and probably occurs in freeze-tolerant species. In the
latter, non-freezing injury could occur either above or
below the SCP, but neither has been carefully studied.
The duration of exposure is an important element in nonfreezing injury and death, as the trauma accumulates with
increasing time and decreasing temperature. If an insect is
warmed to a temperature at which normal metabolic
activity occurs before the trauma is too severe, the injury
may be repaired.
Insects overwintering in habitats with variable, unpredictable temperatures need special adaptations to avoid
both freezing and non-freezing mortality. In these
habitats, freeze-tolerance may be a preferred method of
avoiding freezing injury, and a mechanism to repair nonfreezing injury may be necessary.
There is not yet consensus about the parameters that
should be used to describe the level of resistance to nonfreezing injury or to predict overwintering survival and
the probability of surviving in a new environment.
Parameters that could be useful include:
(1) The lower thermal limit for normal metabolic activity. This may also be the lowest temperature at which
non-freezing cold injury can be repaired.
(2) The neutral or maintenance zone lies between the
lower thermal limit for active metabolism and the highest
temperature at which cold injury occurs (ULCIZ). Within
this zone, neither cold injury nor the repair of previous
cold injury can occur. For insects in habitats with seasonal cold stresses, it includes the optimum temperature
for survival of overwintering insects.
(3) Parameters describing the cold injury zone. The
ULCIZ defines the highest temperature at which cold
injury occurs within a time period reasonable for the
duration of low temperatures in the overwintering habitat.
Defining the lower limit of the cold injury zone is more
complex. Simply, it is the temperature at which cold
injury causes death in a very short time, perhaps 1 day,
but freeze-susceptible insects may die from freezing
before this lower limit is reached. In such cases, the SCP
defines the lower limit of the cold injury zone. Mortality
due to cold injury may occur among freeze-tolerant species both above and below their SCP. Mortality occurs at
temperatures slightly below the SCP, but no data is available as to the cause of this mortality, or the role of duration of exposure in causing it.
(4) The effect of time and temperature within the cold
injury zone can be described by a form of the negative
degree-days, such as SIT. Such an equation would also
provide a mechanism for estimating survival under combinations of time/temperatures within the range of conditions within the habitat, and a prediction of the probable
survival of a species in a new climatic zone. These data
would be useful for all species, regardless of how they
avoid freezing injury.
(5) The mean SCP is useful for some descriptive purposes, but the frequency distribution of the SCPs will be
necessary to predict overwintering survival for some
freeze-susceptible species in habitats in which freezing
intervenes before death from non-freezing injury.
With such data and a knowledge of the temperatures of
exposure, models to predict survival could be prepared.
Different types of winter stresses would require different
approaches to predictive models.
The simplest model would be for species in which
freezing is the main cause of overwintering mortality. The
only parameters in a predictive model of overwintering
survival would be the minimum temperature and the frequency distribution of the SCP. The complete absence of
non-freezing mortality is probably rare, but in some species the proportion dying of such injury under usual exposures might be low enough to ignore in predicting
survival. This model would be most likely to apply to
freeze-susceptible species in exposed habitats in climatic
zones with low temperatures.
In species where non-freezing cold injury is the main
cause of overwintering mortality, the predictive equation
for survival would include both time and temperature.
Various mathematical approaches for predicting survival
such as SIT (negative degree-days), regression analysis,
and other mathematical approaches have been suggested,
but not widely tested (NedvČd, 1998). This approach is
most likely to apply to freeze-susceptible insects overwintering in protected habitats.
Freeze-tolerance has the same effect as lowering the
SCP, it removes freezing injury as a threat to survival.
Predicting survival in habitats in which temperatures
remain below the lower thermal limit would be based
only upon susceptibility to cold injury. Habitats in which
temperatures fluctuate between the cold-injury zone and
above the lower thermal limit for metabolic activity allow
the possibility of repair/reversal of cold injury. Prediction
of survival in such habitats would include information on
the parameters of the repair process.
ACKNOWLEDGEMENTS. The help given by R.A. Raditz and
D. Phillips, Meteorological Service, Environment Canada; W.
Block, British Antarctic Survey; T. Papakyriakou and A. Lan-
glois, Department of Geography, University of Manitoba; D.
Blair, University of Winnipeg; and L. Fishback, Churchill
Northern Studies Centre, Churchill, Manitoba, with the literature on weather, climate, and descriptions of climatic conditions
is gratefully acknowledged. Many friends and colleagues in the
coldhardiness research community, particularly L. Sømme, H.
Ramløv, O. NedvČd and W. Block, have been encouraging and
helpful. Over the years, W.O. Pruitt Jr., Department of Zoology,
University of Manitoba, has shared his knowledge and appreciation of snow, which contributed to the development of this
analysis. N. White and C. Demianyk reviewed the manuscript
before submission.
REFERENCES
BAILEY W.G., OKE T.R. & ROUSE W.R. 1997: The Surface Climates of Canada. McGill-Queens Univ. Press, Montreal &
Kingston, 484 pp.
BALE J.S. 1987: Insect cold hardiness: freezing and supercooling
– an ecophysiological perspective. J. Insect Physiol. 33:
899–908.
BALE J.S. 1991: Insects at low temperature: a predictable relationship? Func. Ecol. 5: 291–298.
BALE J.S. 1993: Classes of insect coldhardiness. Func. Ecol. 7:
751–753.
BALE J.S. 1996: Insect cold hardiness: a matter of life and death.
Eur. J. Entomol. 93: 369–382.
BALE J.S., HARRINGTON R. & CLOUGH M.S. 1988: Low temperature mortality of the peach-potato aphid Myzus persicae.
Ecol. Entomol. 13: 121–129.
BARNES B. & HODSON A.C. 1956: Low temperature tolerance of
the European corn borer in relation to winter survival in Minnesota. J. Econ. Entomol. 49: 19–24.
BAUST J.G. & EDWARDS J.S. 1979: Mechanisms of freezing tolerance in an Antarctic midge, Belgica antarctica. Physiol. Entomol. 4: 1–5.
BAUST J.G. & LEE R.E. JR. 1981: Divergent mechanisms of
frost-hardiness in two populations of the gall fly, Eurosta solidaginis. J. Insect Physiol. 27: 485–490.
BAUST J.G. & MORRISSEY R.E. 1975: Supercooling phenomenon
and water content independence in the overwintering beetle,
Coleomegilla maculata. J. Insect Physiol. 21: 1751–1754.
BAUST J.G., GRANDEE R., CONDON G. & MORRISSEY R.C. 1979:
The diversity of strategies utilized by separate populations of
gall insects. Physiol. Zool. 52: 572–580.
BENNETT L.E. & LEE R.E. JR. 1989: Simulated winter to summer
transition in diapausing adults of the lady beetle (Hippodamia
convergens): supercooling point is not indicative of coldhardiness. Physiol. Entomol. 14: 361–367.
BIRD J.M. & HODKINSON I.D. 1999: Species at the edge of their
range: The significance of the thermal environment for the
distribution of congeneric Craspedolepta species (Sternorrhyncha: Psylloidea) living on Chamerion angustifolium
(Onagraceae). Eur. J. Entomol. 96: 103–109.
BLOCK W. 1982: Supercooling points of insects and mites on the
Antarctic Peninsula. Ecol. Entomol. 7: 1–8.
BROWN R.D. 2000: Northern hemisphere snowcover variability
and change, 1915–1997. J. Climate 13: 2339–2355.
CASAGRANDE R.A. & HAYNES D.L. 1976: A predictive model for
cereal leaf beetle mortality from sub-freezing temperatures.
Envir. Entomol. 5: 761–769.
CLOUDSLEY-THOMPSON J.L. 1962: Microclimates and the distribution of terrestrial arthropods. Annu. Rev. Entomol. 7:
199–222.
CLOUDSLEY-THOMPSON J.L. 1970: Terrestrial Invertebrates. In
Whittow G.C. (ed.): Comparative Physiology of Thermoregu-
573
lation. Vol. I. Academic Press, New York & London, pp.
15–77.
DANKS H.V. 1978: Modes of seasonal adaptation in the insects.
I. Winter survival. Can. Entomol. 110: 1167–1205.
DANKS H.V. 1996: The wider integration of studies of insect
coldhardiness. Eur. J. Entomol. 93: 383–403.
DANKS H.V., KUKAL O. & RING R.A. 1994: Insect
cold-hardiness: insights from the Arctic. Arctic 47: 391–404.
DENLINGER D.L., LEE R.E. JR., YOCUM G.D. & KUKAL O. 1992:
Role of chilling in the acquisition of cold tolerance and the
capacitation to express stress proteins in diapausing pharate
larvae of the Gypsy Moth, Lymantria dispar. Arch. Insect
Biochem. Physiol. 21: 271–280.
DUMAN J.G. 1980: Factors involved in overwintering survival of
the freeze tolerant beetle, Dendroides canadensis. J. Comp.
Physiol. (B) 136: 53–59.
DUMAN J.G. & MONTGOMERY S.L. 1991: Subzero temperature
adaptions in arthropods from the summit of Mauna Kea,
Hawaii. J. Exp. Zool. 259: 409–412.
DYE D.G. 2002: Variability and trends in the annual snow-cover
cycle in Northern Hemisphere land areas, 1972–2000. Hydrol.
Processes 16: 3065–3077.
FIELDS P.G. 1992: The control of stored-product insects and
mites with extreme temperatures. J. Stored Prod. Res. 28:
89–118.
FIELDS P.G. & MCNEIL J.N. 1986: Possible dual cold-hardiness
strategies in Cisseps fulvicollis (Lepidoptera: Arctiidae). Can.
Entomol. 118: 1309–1311.
FIELDS P.G. & MCNEIL J.N. 1988: The cold-hardiness of Ctenucha virginica (Lepidoptera: Arctiidae) larvae, a freezingtolerant species. J. Insect Physiol. 34: 269–277.
FRENCH H.M. & SLAYMAKER O. 1993: Canada’s Cold Environments. McGill-Queens Univ. Press, Montreal & Kingston,
340 pp.
GEHRKEN U. 1984: Winter survival of an adult bark beetle Ips
acuminatus. J. Insect Physiol. 30: 421–429.
GEHRKEN U. 1992: Inoculative freezing and thermal hysteresis in
the adult beetles Ips acuminatus and Rhagium inquisitor. J.
Insect Physiol. 38: 519–524.
GEHRKEN U. & SOUTHON T.E. 1997: Effect of temperature on
coldhardiness and tissue ice formation in the adult Chrysomelid beetle Melasoma collaris L. J. Insect Physiol. 43:
587–593.
GEIGER R. 1950: The Climate near the Ground. Harvard University Press, Cambridge, USA, 482 pp.
GREEN G.W. 1962: Low winter temperatures and the European
pine shoot moth, Rhyacionia buoliana (Schiff.) in Ontario.
Can. Entomol. 94: 314–336.
GRODY N.C. & BASIST A.N. 1996: Global identification of snowcover using SSM/I measurements. Trans. Geosci. Remote
Sensing 34(1): 237–249.
GRUBOR-LAJSIC G., BLOCK W., PALANACKI V. & GLUMAC S. 1991:
Cold hardiness parameters of overwintering diapause larvae
of Ostrinia nubilalis in Vojvodina, Yugoslavia. Cryo-Letters
12: 177–182.
HANEC W. & BECK S.D. 1960: Cold hardiness in the European
corn borer, Pyrausta nubilalis (Hübn.). J. Insect Physiol. 5:
169–180.
HANSEN T. & MERIVEE E. 1971: Cold hardiness of the cabbage
butterflies Pieris brassicae L. and Pieris rapae L. Eesti NSV
Tead. Akad. Toim. Biol. 20: 298–303.
HODKOVÁ M. & HODEK I. 1994: Control of diapause and supercooling by the retrocerebral complex in Pyrrhocoris apterus.
Entomol. Exp. Appl. 70: 237–245.
574
JING X.H. & KANG L. 2003. Geographical variation in egg coldhardiness: a study on the adaptation strategies of the migratory locust, Locusta migratoria L. Ecol. Entomol. 28:
151–158.
JOHNSON S.L. & LEE R.E. JR. 1990: Regulation of supercooling
and nucleation in a freeze intolerant beetle (Tenebrio
molitor). Cryobiology 27: 562–568.
KALUSHKOV P. & NEDVċD O. 2000: Coldhardiness of Pyrrhocoris
apterus (Heteroptera: Pyrrhocoridae) from central and
southern Europe. Eur. J. Entomol. 97: 149–153.
KING J.C. & TURNER J. 1997: Antarctic Meteorology and Climatology. Cambridge University Press, 425 pp.
KLOK C.J. & CHOWN S.L. 1997: Critical thermal limits, temperature tolerance and water balance of a sub-antarctic caterpillar,
Pringleophaga marioni (Lepidoptera: Tineidae). J. Insect
Physiol 43: 685–694.
KÖPPEN W. 1931: Grundriss der Klimakunde. De Gruyter,
Berlin, 380 pp.
KOPVILLEM H. & KUUSIK A. 1971: On the cold-hardiness of overwintering eggs of the European pine sawfly, Neodiprion sertifer (Geoffr.) and its parasite Achrysocharella ruforum
(Krausse). Eesti NSV Tead. Akad. Toim. Biol. 20: 291–297.
KOŠġÁL V. 1993: Cold-hardiness and supercooling capacity in
diapausing and nondiapausing stages of the cabbage root fly
Delia radicum. Cryobiology 30: 524–531.
LAMB R.J., TURNOCK W.J. & HAYHOE H.N. 1985: Winter survival
and outbreaks of Bertha armyworm, Mamestra configurata
(Lepidoptera: Noctuidae), on canola. Can. Entomol. 117:
727–736.
LARSEN K.H., LEE R.E. JR. & NAULT L.R. 1993: Influence of
developmental conditions on coldhardiness of adult Dalbulus
leafhoppers: implications for overwintering. Entomol. Exp.
Appl. 67: 99–108.
LEE R.E. JR. 1980: Physiological adaptations of Coccinellidae to
supranivean and subnivean hibernacula. J. Insect Physiol. 26:
138–138.
LEE R.E. JR. 1989: Insect cold-hardiness: to freeze or not to
freeze. Bioscience 39: 308–313.
LOZINA-LOZINSKII L.K. 1974: Studies in Cryo-Biology. John
Wiley, New York, 259 pp.
MACPHEE A.W. 1964: Cold-hardiness, habitat, and winter survival of some orchard arthropods in Nova Scotia. Can. Entomol. 96: 617–625.
MADRID F.J. & STEWART R.K. 1981: Ecological significance of
coldhardiness and winter mortality of eggs of the Gypsy Moth
Lymantria dispar L., in Quebec. Envir. Entomol. 10: 586–589.
MERIVEE E. 1978: Cold-Hardiness in Insects. Acad. Sci. Estonian SSR, Tallin, 188 pp. (in Estonian, English abstr.).
MILLER L.K. 1969: Freezing tolerance in an adult insect. Science 166: 105–106.
MILLER L.K. 1982: Coldhardiness strategies of some adult and
immature insects overwintering in Interior Alaska. Comp.
Biochem. Physiol. (A) 73: 595–604.
NEDVċD O. 1993: Comparison of coldhardiness in two ladybird
beetles (Coleoptera: Coccinellidae) with contrasting hibernation behavior. Eur. J. Entomol. 90: 465–470.
NEDVċD O. 1998: Modelling the relationship between cold injury
and accumulated degree days in terrestrial arthropods. CryoLetters 19: 267–274.
NEDVċD O. 2000a: Chill tolerance in the tropical beetle Stenotarsus rotundus. Cryo-Letters 21: 25–30.
NEDVċD O. 2000b: Snow White and the seven dwarfs: a multivariate approach to classification of cold tolerance. CryoLetters 21: 339–0348.
NEDVċD O., LAVY D. & VERHOEF H.A. 1998: Modelling the timetemperature relationship in cold injury and effect of hightemperature interruptions on survival in a chill-sensitive
collembolan. Func. Ecol. 12: 816–824.
O’DOHERTY R. & BALE J.S. 1985: Factors affecting coldhardiness of the peach-potato aphid Myzus persicae. Ann. Appl.
Biol. 106: 219–228.
OHYAMA Y. & ASAHINA E. 1972: Frost resistance in adult insects.
J. Insect Physiol. 18: 267–282.
OKE T.R. 1987: Boundary Layer Climates. 2nd ed. Methuen,
London, 435 pp.
OLSEN T.M. & DUMAN J.G. 1997: Maintenance of the supercooled state in the gut fluid of overwintering pyrochroid
beetle larvae, Dendroides canadensis: role of ice nucleators
and antifreeze proteins. J. Comp. Physiol. (B) 167: 114–127.
PANTYUKHOV G.A. 1964: The effect of low temperatures on different populations of the Brown-tail Moth Euproctis chrysorrhoea (L.) and the Gypsy Moth Lymantrria dispar (L.)
(Lepidoptera: Orgyidae). Entomol. Rev. 43: 47–65.
PANTYUKHOV G.A. 1971: Coldhardiness in some species of Coccinellidae. In Maavara V. (ed.): Coldhardiness in Insects and
Mites. Abstracts from a Symposium Held in Tartu (Estonian
SSR) April 19 to 21, 1971. Academy of Sciences of the Estonian SSR, Tartu, pp. 103–108 (in Russian).
PULLIN A.S. & BALE J.S. 1989: Influence of diapause and temperature on cryoprotectant synthesis and coldhardiness in
pupae of Pieris brassicae. Comp. Biochem. Physiol. (A) 94:
499–503.
PULLIN A.S., BALE J.S. & FONTAINE X.L.R. 1991: Physiological
aspects of diapause and cold tolerance during overwintering
in Pieris brassicae. Physiol. Entomol. 16: 447–556.
RAMLØV H. 1999: Microclimate and variations in haemolymph
composition in the freezing-tolerant New Zealand alpine weta
Heimideina maori Hutton (Orthoptera: Stenopelmatidae). J.
Comp. Physiol. (B) 169: 224–235.
RAMLØV H. 2000: Aspects of natural cold tolerance in ectothermic animals. Human Reprod. 15 (Suppl. 5): 26–46.
RENAULT D., SALIN C., VANNIER G. & VERNON P. 2002: Survival
at low temperatures in insects: what is the significance of the
supercooling point. Cryo-Letters 23: 217–228.
RICKARDS J., KELLEHER R.J. & STOREY K.B. 1987: Strategies of
freeze avoidance in larvae of the goldenrod gall moth Epiblemma scudderiana: winter profiles of a natural population.
J. Insect Physiol. 33: 443–450.
RING R.A. 1982: Freezing-tolerant insects with low supercooling
points. Comp. Biochem. Physiol. (A) 73: 605–612.
RING R.A. & TESAR D. 1980: Coldhardiness of the Arctic beetle
Pytho americanus Kirby, Coleoptera, Pythidae (Salpingidae).
J. Insect Physiol. 26: 763–774.
ROBERTS S.J., ARMBRUST E.J. & SELL D.K. 1972: Supercooling
points of several species of Lepidoptera found on soybeans.
Envir. Entomol. 1: 671–672.
SAKAGAMI S.F., TANNO K., TSUTSUI H. & HONMA K. 1985. The
role of cocoons in overwintering of the Soybean Pod Borer
Leguminivora glycinivorella (Lepidoptera: Tortricidae). J.
Kans. Entomol. Soc. 58: 240–247.
SALT R.W. 1959: Role of glycerol in the cold-hardening of
Bracon cephi (Gahan). Can. J. Zool. 37: 59–69.
SATVELD O. 1975: Overvintringsbiologien tilden skarptannete
barkbillen Ips acuminatus Gyll. (Coleoptera: Scolytidae) med
særlig vekt på kuldetoleranse. University of Oslo, 112 pp.
SHEL’DESHOVA G.G. 1967: Ecological factors determining distribution of the Codling Moth Laspeyresia pomonella L. (Lepidoptera, Tortricidae) in the northern and southern
hemispheres. Entomol. Rev. 46: 349–360.
SHIMADA K., SAKAGAMI S.F., HONMA K. & TSUTSUI H. 1984: Seasonal changes of glycogen/trehalose contents, supercooling
points, and survival rate in mature larvae of the overwintering
Soybean Pod Borer Leguminivora glycinivorella. J. Insect
Physiol. 30: 369–373.
SHINTANI Y. & ISHIKAWA Y. 1999. Geographic variation in coldhardiness of eggs and neonate larvae of the yellow-spotted
longicorn beetle, Psacothea hilaris. Physiol. Entomol. 24:
158–164.
SINCLAIR B.J. 1999: Insect cold tolerance: How many kinds of
frozen? Eur. J. Entomol. 96: 157–164.
SINCLAIR B.J. 2001: Field ecology of cold tolerance: interannual
variation in cooling rates, freeze-thaw and thermal stress in
the microhabitat of the alpine cockroach Celatoblatta quinquemaculata. Oikos 93: 286–293.
SINCLAIR B.J., ADDO-BEDIAKO A., CHOWN S.L. 2003: Climatic
variability and the evolution of insect freeze tolerance. Biol.
Rev. 78: 181–195.
SØMME L. 1964: Effects of glycerol on cold-hardiness in insects.
Can. J. Zool. 42: 87–101.
SØMME L. 1965: Further observations on glycerol and coldhardiness in insects. Can. J. Zool. 43: 765–770.
SØMME L. 1967: The effect of temperature and anoxia on
haemolymph composition and supercooling in three overwintering insects. J. Insect Physiol. 13: 805–814.
SØMME L. 1978: Nucleating agents in the haemolymph of third
instar larvae of Eurosta solidaginis (Fitch) (Dipt.,
Tephritidae). Norw. J. Entomol. 25: 187–188.
SØMME L. 1982: Supercooling and winter survival in terrestrial
arthropods. Comp. Biochem. Physiol. (A) 73: 519–543.
SØMME L. 1999: The physiology of cold hardiness in terrestrial
arthropods. Eur. J. Entomol. 96: 1–10.
SØMME L. & ZACHARIASSEN K.E. 1981: Adaptations to low temperatures in high altitude insects from Mount Kenya. Ecol.
Entomol. 6: 199–204.
STOREY K.B. & STOREY J.M. 1987. Freeze tolerance: constraining forces, adaptive mechanisms. Can. J. Zool. 66:
1122–1127.
SULLIVAN C.R. 1965: Laboratory and field investigations on the
ability of eggs of the European pine sawfly, Neodiprion sertifer (Geoffroy) to withstand low temperatures. Can. Entomol.
97: 978–993.
SULLIVAN C.R. & WALLACE D.R. 1972: The potential northern
dispersal of the Gypsy Moth, Porthetria dispar (Lepidoptera:
Lymantriidae). Can. Entomol. 104: 1349–1345.
TAUBER M.J., TAUBER C.A. & MASAKI S. 1986: Seasonal Adaptations of Insects. Oxford University Press, New York, 411 pp.
TENOW O. & NILSSEN A. 1990: Egg cold hardiness and topoclimatic limitations to outbreaks of Epirrita autumnata in
northern Fennoscandia. J. Appl. Ecol. 27: 723–734.
TREWARTHA G.T. & HORN L.H. 1980: An Introduction to
Climate. McGraw-Hill, New York, 416 pp.
TRUCHAN J. & BUTCHER J.W. 1970: Coldhardiness of Dendrosoter protuberans. J. Econ. Entomol. 63: 328–330.
TSUTSUI H., TANNO K. & TORIKURA H. 1987: Coldhardiness of
overwintering eggs in Celaena leucostigma and Amphipoea
fucosa (Lepidoptera: Noctuidae). Jap. J. Appl. Entomol. Zool.
31: 261–263.
TURNOCK W.J. 1993: Cold-hardiness of Lacanobia atlantica
(Lepidoptera: Noctuidae), and a comparison with three other
insect species that overwinter in the same habitat. Can. J.
Zool. 71: 1710–1714.
TURNOCK W.J. & BILODEAU R.J. 1992: Life history and coldhardiness of Athrycia cinerea (Dipt.: Tachinidae) in western
Canada. Entomophaga 37: 353–362.
575
TURNOCK W.J. & BODNARYK R.P. 1991: Latent cold injury and
its conditional expression in the Bertha armyworm, Mamestra
configurata (Noctuidae: Lepidoptera). Cryo-Letters 12:
377–384.
TURNOCK W.J. & BODNARYK R.P. 1993: The reversal of cold
injury and its effect on the response to subsequent cold exposures. Cryo-Letters 14: 251–256.
TURNOCK W.J. & CARL K.P. 1995: Evaluation of the Palaearctic
Eurithia consobrina (Diptera: Tachinidae) as a potential biocontrol agent for Mamestra configurata (Lepidoptera: Noctuidae) in Canada. Biocontrol Sci. Technol. 5: 55–67.
TURNOCK W.J., LAMB R.J. & BODNARYK R.P. 1983: Effects of
cold stress during diapause on the survival and development
of Mamestra configurata (Lepidoptera: Noctuidae). Oecologia 56: 185–192.
TURNOCK W.J., JONES T.H. & READER P.M. 1985: Effects of cold
stress during diapause on the survival and development of
Delia radicum (Diptera; Anthomyiidae) in England. Oecologia 67: 506–510.
TURNOCK W.J., READER P.M. & BRACKEN G.K. 1990: A comparison of the coldhardiness of populations of Delia radicum
(L.) (Diptera: Anthomyiidae) from southern England and the
Canadian prairies. Can. J. Zool. 68: 830–835.
TURNOCK W.J., BOIVIN G. & RING R.A. 1998: Interpopulation
differences in the coldhardiness of Delia radicum (Diptera:
Anthomyiidae). Can. Entomol. 130: 119–129.
VAN DER LAAK S. 1982: Physiological adaptations to low temperature in freezing-tolerant Phyllodecta laticollis beetles.
Comp. Biochem. Physiol. (A) 73: 613–620.
VAN DER WOUDE & VERHOEF H.A. 1986: A comparative study of
winter survival in two temperate Collembola. Ecol. Entomol.
11: 333–340.
VERNON P., VANNIER G. & LUCE J.-M. 1996: Découverte de
larves tolérantes et intolérantes à la congélation dans une
même guilde de Cétoines (Coléoptères) en forêt de Fountainebleau. Écologie 27: 131–142.
WERNER R.A. 1978: Overwinter survival of spear-marked black
moth, Pheumaptera hastata (Lepidoptera: Geometridae),
pupae in interior Alaska. Can. Entomol. 110: 877–882.
ZACHARIASSEN K.E. 1977: Effects of glycerol in freeze-tolerant
Pytho depressus L. (Col., Pythidae). Norw. J. Entomol. 24:
25–29.
ZACHARIASSEN K.E. 1980: The role of polyols and nucleating
agents in cold-hardy beetles. J. Comp. Physiol. 140: 227–234.
ZACHARIASSEN K.E. & HAMMEL H.T. 1976: Nucleating agents in
the haemolymph of insects tolerant to freezing. Nature 262:
285–287.
Received February 11, 2005; revised and accepted June 14, 2005
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